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Fungal endophytes from seeds of invasive, non-native Phragmites australis and their potential role in germination and seedling growth

Background and aims We characterized fungal endophytes of seeds of invasive, non-native Phragmites from three sites in the Great Lakes region to determine if fungal symbiosis could contribute to invasiveness through their effects on seed germination and seedling growth. Methods Field-collected seeds were surface sterilized and plated on agar to culture endophytes for ITS sequencing. Prevalence of specific endophytes from germinated and non-germinated seeds, and from seedlings, was compared. Results One-third of 740 seeds yielded endophyte isolates. Fifteen taxa were identified with Alternaria sp. representing 54% of all isolates followed by Phoma sp. (21%) and Penicillium corylophilum (12%). Overall germination of seeds producing an isolate (36%) was significantly higher than seeds not producing an isolate (20%). Penicillium in particular was strongly associated with increased germination of seeds from one site. Sixty-three isolates and 11 taxa were also obtained from 30 seedlings where Phoma , Penicillium and Alternaria respectively were most prevalent. There was a significant effect of isolating an endophyte from the seed on seedling growth. Conclusions These results suggest that many endophyte taxa are transmitted in seeds and can increase seed germination and seedling growth of invasive Phragmites . The role of fungal endophytes in host establishment, growth and invasiveness in nature requires further research.

Michigan, Ohio

Microbial disease and the coral holobiont

Tropical coral reefs harbour a reservoir of enormous biodiversity that is increasingly threatened by direct human activities and indirect global climate shifts. Emerging coral diseases are one serious threat implicated in extensive reef deterioration through disruption of the integrity of the coral holobiont – a complex symbiosis between the coral animal, endobiotic alga and an array of microorganisms. In this article, we review our current understanding of the role of microorganisms in coral health and disease, and highlight the pressing interdisciplinary research priorities required to elucidate the mechanisms of disease. We advocate an approach that applies knowledge gained from experiences in human and veterinary medicine, integrated into multidisciplinary studies that investigate the interactions between host, agent and environment of a given coral disease. These approaches include robust and precise disease diagnosis, standardised ecological methods and application of rapidly developing DNA, RNA and protein technologies, alongside established histological, microbial ecology and ecological expertise. Such approaches will allow a better understanding of the causes of coral mortality and coral reef declines and help assess potential management options to mitigate their effects in the longer term.

Trends in Microbiology

Coral adaptation and acclimatization: A most ingenious paradox

Reef corals and the communities they form evidently possess effective mechanisms of adaptation and acclimation that have ensured their survival and recurrence over geologic time. Current reef degradation suggests that these mechanisms are being taxed beyond their limits; understanding of the problem is hampered by serious inadequacies in our understanding of physiological stress responses, the range and implications of reproductive strategies, and the mechanisms of calcification and algal symbiosis. Reef community and population responses to environmental change appear substantially different on different time scales, and a combination of short-term perspectives and definitional confusion complicates interpretation and prediction of reef responses. Calcium carbonate saturation state is now recognized as a potentially important control of reef calcification, which means that rising atmospheric CO 2 represents a direct threat to reef ecosystems on a global scale.

American Zoologist

Manipulation of the Symbiodiniaceae microbiome confers multigenerational impacts on symbioses and reproductive ecology of its Exaiptasia diaphana host

Symbiodiniaceae-associated microbiota strongly influence cnidarian symbioses. We systematically reduced the bacterial and fungal communities associated with Symbiodiniaceae to study potential effects on the cnidarian holobiont Exaiptasia diaphana (Aiptasia). Clonal anemones were inoculated with xenic Breviolum minutum (SSB01) and microbiome-manipulated cultures after antibacterial or antifungal treatment. The asexual reproduction of pedal laceration allowed for three generations of clonal aposymbiotic Aiptasia to be utilised in this study, from the initial adult generation (G0), to the first (G1), and second (G2) generation. We inoculated small and large G1 Aiptasia with SSB01 algae and monitored onset of symbiosis, rate of algal proliferation, and holobiont characteristics. Sequencing the 16S and 18S rRNA gene regions identified significant differences in the bacterial and fungal communities of the G0 and G1 generations, alongside differences between the size classes of small and large G1 anemones. The microbiome of larger G1 individuals was distinct to the smaller G1 anemones, suggesting a microbiome maturation process. Control Breviolum minutum cultures exhibited a significantly greater proliferation rate in large G1 anemones when compared to antibacterial or antifungal treated cultures, whereas the opposite trend was documented in the small G1 anemones. Although no differences were observed between algal photochemical parameters, or the growth and polyp activity of G1 juveniles, we observed a significant influence in the production of G2 clones between treatments. Overall, we provide strong ecological implications of manipulating Symbiodiniaceae microbiome, not for the algae themselves, but for the maturation of the host Aiptasia, as well as for the cnidarian holobiont over multiple generations.

The ISME Journal

Experimental warming alters free-living nitrogen fixation in a humid tropical forest

Microbial nitrogen (N) fixation accounts for c. 97% of natural N inputs to terrestrial ecosystems. These microbes can be free-living in the soil and leaf litter (asymbiotic) or in symbiosis with plants. Warming is expected to increase N-fixation rates because warmer temperatures favor the growth and activity of N-fixing microbes. We investigated the effects of warming on asymbiotic components of N fixation at a field warming experiment in Puerto Rico. We analyzed the function and composition of bacterial communities from surface soil and leaf litter samples. Warming significantly increased asymbiotic N-fixation rates in soil by 55% (to 0.002 kg ha −1 yr −1 ) and by 525% in leaf litter (to 14.518 kg ha −1 yr −1 ) . This increase in N fixation was associated with changes in the N-fixing bacterial community composition and soil nutrients. Our findings suggest that warming increases the natural N inputs from the atmosphere into this tropical forest due to changes in microbial function and composition, especially in the leaf litter. Given the importance of leaf litter in nutrient cycling, future research should investigate other aspects of N cycles in the leaf litter under warming conditions.

Luquillo Experimental Forest, northeastern Puerto

Cement manufacture and the environment - Part I: Chemistry and technology

Hydraulic (chiefly portland) cement is the binding agent in concrete and mortar and thus a key component of a country's construction sector. Concrete is arguably the most abundant of all manufactured solid materials. Portland cement is made primarily from finely ground clinker, which itself is composed dominantly of hydraulically active calcium silicate minerals formed through high-temperature burning of limestone and other materials in a kiln. This process requires approximately 1.7 tons of raw materials perton of clinker produced and yields about 1 ton of carbon dioxide (CO2) emissions, of which calcination of limestone and the combustion of fuels each contribute about half. The overall level of CO2 output makes the cement industry one of the top two manufacturing industry sources of greenhouse gases; however, in many countries, the cement industry's contribution is a small fraction of that from fossil fuel combustion by power plants and motor vehicles. The nature of clinker and the enormous heat requirements of its manufacture allow the cement industry to consume a wide variety of waste raw materials and fuels, thus providing the opportunity to apply key concepts of industrial ecology, most notably the closing of loops through the use of by-products of other industries (industrial symbiosis). In this article, the chemistry and technology of cement manufacture are summarized. In a forthcoming companion article (part II), some of the environmental challenges and opportunities facing the cement industry are described. Because of the size and scope of the U.S. cement industry, the analysis relies primarily on data and practices from the United States.

Journal of Industrial Ecology

Can differences in phosphorus uptake kinetics explain the distribution of cattail and sawgrass in the Florida Everglades?

Background Cattail ( Typha domingensis ) has been spreading in phosphorus (P) enriched areas of the oligotrophic Florida Everglades at the expense of sawgrass ( Cladium mariscus spp. jamaicense ). Abundant evidence in the literature explains how the opportunistic features of Typha might lead to a complete dominance in P-enriched areas. Less clear is how Typha can grow and acquire P at extremely low P levels, which prevail in the unimpacted areas of the Everglades. Results Apparent P uptake kinetics were measured for intact plants of Cladium and Typha acclimated to low and high P at two levels of oxygen in hydroponic culture. The saturated rate of P uptake was higher in Typha than in Cladium and higher in low-P acclimated plants than in high-P acclimated plants. The affinity for P uptake was two-fold higher in Typha than in Cladium , and two- to three-fold higher for low-P acclimated plants compared to high-P acclimated plants. As Cladium had a greater proportion of its biomass allocated to roots, the overall uptake capacity of the two species at high P did not differ. At low P availability, Typha increased biomass allocation to roots more than Cladium . Both species also adjusted their P uptake kinetics, but Typha more so than Cladium . The adjustment of the P uptake system and increased biomass allocation to roots resulted in a five-fold higher uptake per plant for Cladium and a ten-fold higher uptake for Typha . Conclusions Both Cladium and Typha adjust P uptake kinetics in relation to plant demand when P availability is high. When P concentrations are low, however, Typha adjusts P uptake kinetics and also increases allocation to roots more so than Cladium , thereby improving both efficiency and capacity of P uptake. Cladium has less need to adjust P uptake kinetics because it is already efficient at acquiring P from peat soils (e.g., through secretion of phosphatases, symbiosis with arbuscular mycorrhizal fungi, nutrient conservation growth traits). Thus, although Cladium and Typha have qualitatively similar strategies to improve P-uptake efficiency and capacity under low P-conditions, Typha shows a quantitatively greater response, possibly due to a lesser expression of these mechanisms than Cladium . This difference between the two species helps to explain why an opportunistic species such as Typha is able to grow side by side with Cladium in the P-deficient Everglades.

Florida

Shell microstructure of the late Carboniferous rostroconch mollusc Apotocardium lanterna (Branson, 1965)

The Late Carboniferous bransoniid conocardioidean Apotocardium lanterna ( Branson, 1965 ) had an entirely aragonitic shell with a finely prismatic outer shell layer, a predominantly crossed lamellar to complex crossed lamellar middle shell layer, and an “inner” shell layer of finely textured porcelaneous and/or matted structure. This “inner” layer is probably homologous with the inner part of the middle shell layer and the inner layer sensu stricto of bivalved molluscs. Shell morphological and microstructural convergences between conocardioids and living heart cockles suggest that at least some conocardioids may have farmed algal endosymbionts in their posterior mantle margins. This symbiosis may have helped conocardioids compete with the biomechanically more efficient bivalves during the latter part of the Paleozoic.

Journal of Paleontology

Phoretic sharksuckers (Echeneis naucrates) associated with an elasmobranch host occupy higher relative trophic positions

The relationship between phoretic diskfishes and their hosts is a classic example of marine symbiosis, yet surprisingly few studies have quantified this trophic relationship. We investigated the hypothesis that by consuming host parasites and prey scraps phoretic diskfishes (Echeneidae) feed at a higher relative trophic position than free-living individuals through expanded foraging opportunities. We used carbon and nitrogen stable isotope analysis of muscle tissue from both free-living and commensal sharksuckers Echeneis naucrates and their hosts, supplemented with gut-content analysis, to investigate this hypothesis. Our analysis revealed that commensal sharksuckers likely occupy higher relative trophic positions than free-living sharksuckers. The importance of scavenging host prey decreased ontogenetically as sharksuckers shifted from symbiotic phoresis to free-swimming behavior, leading to an ontogenetic change in which obligately commensal juveniles occupy higher trophic positions than free-living adults which are only facultatively commensal. Relative differences in δ 13 C and δ 15 N among individual host-commensal pairs varied among host species, suggesting potential differences in foraging opportunities among host taxa.

Marine Ecology Progress Series

Physiological differences in bleaching response of the coral Porites astreoides along the Florida Keys reef tract during high-temperature stress

The Florida Keys reef tract (FKRT) has a unique geological history wherein Holocene sea-level rise and bathymetry interacted, resulting in a reef-building system with notable spatial differences in reef development. Overprinted on this geologic history, recent global and local stressors have led to degraded reefs dominated by fleshy algae, soft corals, and sponges. Here, we assessed how coral physiology (calcification rate, tissue thickness, reproduction, symbiosis, and bleaching) varies seasonally (winter vs. summer) and geographically using 40 colonies of the mustard hill coral Porites astreoides from four sites across 350 km along the FKRT from 2015 to 2017. The study coincided with a high-temperature event in late summer 2015 that caused heterogeneous levels of coral bleaching across sites. Bleaching severity differed by site, with bleaching response more aligned with heat stress retroactively calculated from local degree heating weeks than those predicted by satellites. Despite differences in temperature profiles and bleaching severity, all colonies hosted Symbiodiniaceae of the same genus (formerly Clade A and subtypes). Overall, P. astreoides at Dry Tortugas National Park, the consistently coolest site, had the highest calcification rates, symbiont cell densities, and reproductive potential (all colonies were reproductive, with most planula larvae per polyp). Corals at Dry Tortugas and Fowey Rocks Light demonstrated strong seasonality in net calcification (higher in summer) and did not express visual or partial-mortality responses from the bleaching event; in contrast, colonies in the middle and southern part of the upper keys, Sombrero Key and Crocker Reef, demonstrated similar reduced fitness from bleaching, but differential recovery trajectories following the heat stress. Identifying reefs, such as Dry Tortugas and possibly Fowey Rocks Light that may serve as heat-stress refugia, is important in selecting candidate sites for adaptive reef-management strategies, such as selective propagation and assisted gene flow, to increase coral-species adaptation to ocean warming.

Florida

Viral-like particles are associated with endosymbiont pathology in Florida corals affected by stony coral tissue loss disease

Stony coral tissue loss disease (SCTLD) was first documented in 2014 near the Port of Miami, Florida, and has since spread north and south along Florida’s Coral Reef, killing large numbers of more than 20 species of coral and leading to the functional extinction of at least one species, Dendrogyra cylindrus . SCTLD is assumed to be caused by bacteria based on presence of different molecular assemblages of bacteria in lesioned compared to apparently healthy tissues, its apparent spread among colonies, and cessation of spread of lesions in individual colonies treated with antibiotics. However, light microscopic examination of tissues of corals affected with SCTLD has not shown bacteria associated with tissue death. Rather, microscopy shows dead and dying coral cells and symbiotic dinoflagellates (endosymbionts) indicating a breakdown of host cell and endosymbiont symbiosis. It is unclear whether host cells die first leading to death of endosymbionts or vice versa. Based on microscopy, hypotheses as to possible causes of SCTLD include infectious agents not visible at the light microscopy level or toxicosis, perhaps originating from endosymbionts. To clarify this, we examined corals affected with SCTLD and apparently healthy corals using transmission electron microscopy. Endosymbionts in SCTLD-affected and apparently healthy corals consistently had varying degrees of pathology associated with elongated particles compatible in morphology with filamentous positive single-stranded RNA viruses of plants termed anisometric viral-like particles (AVLP). There was apparent progression from early to late replication of AVLP in the cytoplasm of endosymbionts adjacent to or at times within chloroplasts, with morphologic changes in chloroplasts consistent with those seen in plant cells infected by viruses. Coral host cell pathology appeared limited to massive proliferation and lysis of mucus cells. Based on these findings, we hypothesize that SCTLD is a viral disease of endosymbionts leading to coral host death. Efforts to confirm the presence of a virus associated with SCTLD through other means would be appropriate. These include showing the presence of a virus through molecular assays such as deep sequencing, attempts to grow this virus in the laboratory through culture of endosymbionts, localization of virus in tissue sections using immunohistochemistry or in situ hybridization, and experimental infection of known-virus-negative corals to replicate disease at the gross and microscopic level.

Florida

Effects of host injury on susceptibility of marine reef fishes to ectoparasitic gnathiid isopods

The importance of the role that parasites play in ecological communities is becoming increasingly apparent. However much about their impact on hosts and thus populations and communities remains poorly understood. A common observation in wild populations is high variation in levels of parasite infestation among hosts. While high variation could be due to chance encounter, there is increasing evidence to suggest that such patterns are due to a combination of environmental, host, and parasite factors. In order to examine the role of host condition on parasite infection, rates of Gnathia marleyi infestation were compared between experimentally injured and uninjured fish hosts. Experimental injuries were similar to the minor wounds commonly observed in nature. The presence of the injury significantly increased the probability of infestation by gnathiids. However, the level of infestation (i.e., total number of gnathiid parasites) for individual hosts, appeared to be unaffected by the treatment. The results from this study indicate that injuries obtained by fish in nature may carry the additional cost of increased parasite burden along with the costs typically associated with physical injury. These results suggest that host condition may be an important factor in determining the likelihood of infestation by a common coral reef fish ectoparasite, G. marleyi .

Symbiosis